Abstract
A genome led phylophasic study was designed to determine the taxonomic status of a strain, DSM 45956, recovered from a Saharan desert soil. A wealth of taxonomic data, including average nucleotide identity and DNA:DNA hybridization (DDH) values, showed that the isolate and the type strains of Actinopolyspora lacussalsi and Actinopolyspora righensis belong to the same species. Consequently, it is proposed that A. righensis is a heterotypic synonym of A. lacussalsi. Similarly, DDH values and associated phenotypic data show that A. lacussalsi contains two subspecies, A. lacussalsi subsp. lacussalsi and A. lacussalsi subsp. righensis which includes isolate DSM 45956.
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Data availability
The GenBank accession numbers for the 16S rRNA gene sequence of strain DSM 45956 is KJ574193.1. The genomics datasets used during the current study are available at the JGI website (https://img.jgi.doe.gov) with accession codes SAMN04487904 (A. righensis), SAMN18243356 (A. lacussalsi), SAMN10872242 (strain DSM 45956) and SAMN04487820 (A. mzabensis).
References
Arulprakasam KR, Dharumadurai D (2021) Genome mining of biosynthetic gene clusters intended for secondary metabolites conservation in actinobacteria. Microb Pathog 161:105252. https://doi.org/10.1016/j.micpath.2021.105252
Becker B, Lechevalier MP, Gordon RE, Lechevalier HA (1964) Rapid differentiation between Nocardia and Streptomyces by paper chromatography of whole-cell hydrolysates. J Appl Microbiol 12:421–423. https://doi.org/10.1128/am.12.5.421-423.1964
Blin K, Shaw S, Kloosterman AM, Charlop-Powers Z, van Wezel GP, Medema MH, Weber T (2021) antiSMASH 6.0: Improving cluster detection and comparison capabilities. Nucleic Acids Res 49:W29–W35. https://doi.org/10.1093/nar/gkab335
Boudjelal F, Zitouni A, Mathieu F, Lebrihi A, Sabaou N (2011) Taxonomy and antimicrobial activities of two novel halophilic Saccharomonospora strains isolated in Algerian Sahara soils. Ann Microbiol 61:299–305. https://doi.org/10.1007/s13213-010-0138-9
Chen D, Feng J, Huang L, Zhang Q, Wu J, Zhu X, Duan Y, Xu Z (2014) Identification and characterization of a new erythromycin biosynthetic gene cluster in Actinopolyspora erythraea YIM90600, a novel erythronolide-producing halophilic actinomycete isolated from salt field. PLoS One. https://doi.org/10.1371/journal.pone.0108129
Chun J, Bae KS, Moon EY, Jung SO, Lee HK, Kim SJ (2000) Nocardiopsis kunsanensis sp. nov., a moderately halophilic actinomycete isolated from a saltern. Int J Syst Evol Microbiol 50:1909–1913. https://doi.org/10.1099/00207713-50-5-1909
Chun J, Oren A, Ventosa A, Christensen H, Arahal DR, da Costa MS, Rooney AP, Yi H, Xu XW, De Meyer S, Trujillo ME (2018) Proposed minimal standards for the use of genome data for the taxonomy of prokaryotes. Int J Syst Evol Microbiol 68:461–466. https://doi.org/10.1099/ijsem.0.002516
Duangmal K, Suksaard P, Pathom-aree W, Mingma R, Matsumoto A, Takahashi Y (2016) Actinopolyspora salinaria sp. nov., a halophilic actinomycete isolated from solar saltern soil. Int J Syst Evol Microbiol 66:1660–1665. https://doi.org/10.1099/ijsem.0.000926
Farris JS (1972) Estimating phylogenetic trees from distance matrices. Am Nat 106:645–668
Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376. https://doi.org/10.1007/BF01734359
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783. https://doi.org/10.2307/2408678
Fitch WM (1971) Toward defining the course of evolution: minimum change for a specific tree topology. Syst Zool 20:406–416. https://doi.org/10.2307/2412116
Fox GE, Wisotzkey JD, Jurtshuk P (1992) How close is close: 16S rRNA sequence identity may not be sufficient to guarantee species identity. Int J Syst Bacteriol 42:166–170. https://doi.org/10.1099/00207713-42-1-166
Gochnauer MB, Leppard GG, Komaratat P, Kates M, Novitsky T, Kushner DJ (1975) Isolation and characterization of Actinopolyspora halophila, gen. et sp. nov., an extremely halophilic actinomycete. Can J Microbiol 21:1500–1511. https://doi.org/10.1139/m75-222
Goodfellow M (1971) Numerical taxonomy of some nocardioform bacteria. J Gen Microbiol 69:33–80. https://doi.org/10.1099/00221287-69-1-33
Gordon RE, Barnett DA, Handerhan JE, Pang CHN (1974) Nocardia coeliaca, Nocardia autotrophica, and the nocardin strain. Int J Syst Bacteriol 24:54–63. https://doi.org/10.1099/00207713-24-1-54
Goris J, Konstantinidis KT, Klappenbach JA, Coenye T, Vandamme P, Tiedje JM (2007) DNA–DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 57:81–91. https://doi.org/10.1099/ijs.0.64483-0
Guan TW, Liu Y, Zhao K, Xia ZF, Zhang XP, Zhang LL (2010) Actinopolyspora xinjiangensis sp. nov., a novel exteremely halophilic actinomycete isolated from a salt lake in Xinjiang. China Antonie Van Leeuwenhoek 98:447–453. https://doi.org/10.1007/s10482-010-9458-9
Guan TW, Wei B, Zhang Y, Xia ZF, Che ZM, Chen XG, Zhang LL (2013) Actinopolyspora lacussalsi sp. nov., an extremely halophilic actinomycete isolated from a salt lake. Int J Syst Evol Microbiol 63:3009–3013. https://doi.org/10.1099/ijs.0.047167-0
Hayakawa M, Nonomura H (1987) Humic acid-vitamin agar, a new medium for the selective isolation of soil actinomycetes. J Ferment Technol 65:01–509. https://doi.org/10.1016/0385-6380(87)90108-7
Horinouchi S (2007) Mining and polishing of the treasure trove in the bacterial genus Streptomyces. Biosci Biotechnol Biochem 71:283–299. https://doi.org/10.1271/bbb.60627
Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Munro HN (ed) Mammalian protein metabolism, vol 3. Academic press, New York, pp 21–132
Kelly KL (1964) Inter-society color council-national bureau of standards color name charts illustrated with centroid colors. US Government Printing Office, Washington, DC
Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120. https://doi.org/10.1007/BF01731581
Kreft Ł, Botzki A, Coppens F, Vandepoele K, Van Bel M (2017) PhyD3: a phylogenetic tree viewer with extended phyloXML support for functional genomics data visualization. Bioinform 33:2946–2947. https://doi.org/10.1093/bioinformatics/btx324
Kroppenstedt RM (1982) Separation of bacterial menaquinones by HPLC using reverse phase (RP18) and a silver loaded ion exchanger as stationary phases. J Liq Chromatogr 5:2359–2367. https://doi.org/10.1080/01483918208067640
Kroppenstedt RM (1985) Fatty acid and menaquinone analysis of actinomycetes and related organisms. In: Goodfellow M, Minnikin DE (eds) Chemical methods in bacterial systematics. Academic Press, London, pp 173–179
Krügel H, Krubasik P, Weber K, Saluz HP, Sandmann G (1999) Functional analysis of genes from Streptomyces griseus involved in the synthesis of isorenieratene, a carotenoid with aromatic end groups, revealed a novel type of carotenoid desaturase. Biochim Biophys Act 1439:7–64. https://doi.org/10.1016/s1388-1981(99)00075-x
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054
Lechevalier MP, Lechevalier H (1970) Chemical composition as a criterion in the classification of aerobic actinomycetes. Int J Syst Bacteriol 20:435–443. https://doi.org/10.1099/00207713-20-4-435
Lechevalier MP, de Bièvre C, Lechevalier HA (1977) Chemotaxonomy of aerobic actinomycetes: phospholipid composition. Biochem Syst Ecol 5:249–260
Lefort V, Desper R, Gascuel O (2015) FastME 2.0: a comprehensive, cccurate, and fast distance-based phylogeny inference program. Mol Biol Evol 32:2798–2800. https://doi.org/10.1093/molbev/msv150
Liu D, Coloe S, Baird R, Pedersen J (2000) Rapid mini-preparation of fungal DNA for PCR. J Clin Microbiol 38:471–471. https://doi.org/10.1128/JCM.38.1.471-471.2000
Marchal N, Bourdon JL, Richard C (1987) Les milieux de culture pour l’isolement et l’identification biochimique des bactéries. Doin Press, Paris
Meier-Kolthoff JP, Göker M (2019) TYGS is an automated high-throughput platform for state-of-the-art genome-based taxonomy. Nat Commun 10:2182. https://doi.org/10.1038/s41467-019-10210-3
Meier-Kolthoff JP, Auch AF, Klenk HP, Göker M (2013) Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinform 14:60. https://doi.org/10.1186/1471-2105-14-60
Meier-Kolthoff JP, Hahnke RL, Petersen J, Scheuner C, Michael V, Fiebig A, Rohde C, Rohde M, Fartmann B, Goodwin LA, Chertkov O, Reddy T, Pati A, Ivanova NN, Markowitz V, Kyrpides NC, Woyke T, Göker M, Klenk HP (2014) Complete genome sequence of DSM 30083T, the type strain (U5/41T) of Escherichia coli, and a proposal for delineating subspecies in microbial taxonomy. Stand Genom Sci 9:2. https://doi.org/10.1186/1944-3277-9-2
Meklat A, Bouras N, Zitouni A, Mathieu F, Lebrihi A, Schumann P, Spröer C, Klenk HP, Sabaou N (2012) Actinopolyspora algeriensis sp. nov., a novel halophilic actinomycete isolated from a Saharan soil. Extremophiles 16:771–776. https://doi.org/10.1007/s00792-012-0473-9
Meklat A, Bouras N, Zitouni A, Mathieu F, Lebrihi A, Schumann P, Spröer C, Klenk HP, Sabaou N (2013a) Actinopolyspora righensis sp. nov., a novel halophilic actinomycete isolated from Saharan soil in Algeria. Antonie Van Leeuwenhoek 104:301–307. https://doi.org/10.1007/s10482-013-9948-7
Meklat A, Bouras N, Zitouni A, Mathieu F, Lebrihi A, Schumann P, Spröer C, Klenk HP, Sabaou N (2013b) Actinopolyspora saharensis sp. nov., a novel halophilic actinomycete isolated from a Saharan soil of Algeria. Antonie Van Leeuwenhoek 103:771–776. https://doi.org/10.1007/s10482-012-9859-z
Meklat A, Bouras N, Zitouni A, Mathieu F, Lebrihi A, Schumann P, Spröer C, Klenk HP, Sabaou N (2013c) Actinopolyspora mzabensis sp. nov., a halophilic actinomycete isolated from an Algerian Saharan soil. Int J Syst Evol Microbiol 63:3787–3792. https://doi.org/10.1099/ijs.0.046649-0
Meklat A, Bouras N, Zitouni A, Mathieu F, Lebrihi A, Schumann P, Spröer C, Klenk HP, Sabaou N (2014) Saccharopolyspora ghardaiensis sp. nov., an extremely halophilic actinomycete isolated from Algerian Saharan soil. J Antibiot 67:299–303. https://doi.org/10.1038/ja.2013.136
Minnikin DE, Patel PV, Alshamaony L, Goodfellow M (1977) Polar lipid composition in the classification of Nocardia and related bacteria. Int J Syst Bacteriol 27:104–117. https://doi.org/10.1099/00207713-27-2-104
Minnikin DE, Hutchinson IG, Caldicott AB, Goodfellow M (1980) Thin-layer chromatography of methanolysates of mycolic acid-containing bacteria. J Chromatogr A 188:221–233. https://doi.org/10.1016/S0021-9673(00)88433-2
Minnikin DE, O’Donnell AG, Goodfellow M, Alderson G, Athalye M, Schaal A, Parlett JH (1984) An integrated procedure for the extraction of bacterial isoprenoid quinones and polar lipids. J Microbiol Methods 2:233–241. https://doi.org/10.1016/0167-7012(84)90018-6
Nouioui I, Carro L, García-López M, Meier-Kolthoff JP, Woyke T, Kyrpides NC, Pukall R, Klenk HP, Goodfellow M, Göker M (2018) Genome-based taxonomic classification of the phylum Actinobacteria. Front Microbiol. https://doi.org/10.3389/fmicb.2018.02007
Rainey FA, Ward-Rainey N, Kroppenstedt RM, Stackebrandt E (1996) The genus Nocardiopsis represents a phylogenetically coherent taxon and a distinct actinomycete lineage: proposal of Nocardiopsaceae fam. nov. Int J Syst Bacteriol 46:1088–1092. https://doi.org/10.1099/00207713-46-4-1088
Rodriguez-R LM, Konstantinidis KT (2016) The enveomics collection: a toolbox for specialized analyses of microbial genomes and metagenomes. PeerJ Prepr. https://doi.org/10.7287/peerj.preprints.1900v1
Saitou N, Nei M (1987) The neighbour-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425. https://doi.org/10.1093/oxfordjournals.molbev.a040454
Saker R, Bouras N, Meklat A, Zitouni A, Schumann P, Spröer C, Klenk HP, Sabaou N (2015) Actinopolyspora biskrensis sp. nov., a novel halophilic actinomycete isolated from northern Sahara. Curr Microbiol 70:23–428. https://doi.org/10.1007/s00284-014-0740-3
Sasser M (1990) Identification of bacteria by gas chromatography of cellular fatty acids. Technical note 101. Microbial ID, Newark
Shirling EB, Gottlieb D (1966) Methods for characterization of Streptomyces species. Int J Syst Bacteriol 16:313–340. https://doi.org/10.1099/00207713-16-3-313
Solanki R, Khanna M, Lal R (2008) Bioactive compounds from marine actinomycetes. Indian J Microbiol 48:410–431. https://doi.org/10.1007/s12088-008-0052-z
Sooklal SA, De Koning C, Brady D, Rumbold K (2020) Identification and characterisation of a fluorinase from Actinopolyspora mzabensis. Protein Expr Purif 166:105508. https://doi.org/10.1016/j.pep.2019.105508
Stackebrandt E, Goebel BM (1994) Taxonomic note: a place for DNA-DNA reassociation and 16S rRNA sequence analysis in the present species definition in bacteriology. Int J Syst Evol Microbiol 44:846–849. https://doi.org/10.1099/00207713-44-4-846
Tang SK, Wang Y, Klenk HP, Shi R, Lou K, Zhang YJ, Chen C, Ruan JS, Li WJ (2011) Actinopolyspora alba sp. Nov. and Actinopolyspora erythraea sp. Nov., isolated from a salt field, and reclassification of Actinopolyspora iraqiensis Ruan et al. 1994 as a heterotypic synonym of Saccharomonospora halophila. Int J Syst Evol Microbiol 61:1693–1698. https://doi.org/10.1099/ijs.0.022319-0
Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680. https://doi.org/10.1093/nar/22.22.4673
Yoshida M, Matsubara K, Kudo T, Horikoshi K (1991) Actinopolyspora mortivallis sp. nov., a moderately halophilic actinomycete. Int J Syst Bacteriol 41:15–20. https://doi.org/10.1099/00207713-41-1-15
Zhi XY, Li WJ, Stackebrandt E (2009) An update of the structure and 16S rRNA gene sequence-based definition of higher ranks of the class Actinobacteria, with the proposal of two new suborders and four new families and emended descriptions of the existing higher taxa. Int J Syst Evol Microbiol 59:589–608. https://doi.org/10.1099/ijs.0.65780-0
Acknowledgements
We thank the late Prof. N. Sabaou (LBSM, Ecole Normale Supérieure de Kouba, Algiers, Algeria) for great help in the isolation and taxonomic analysis of strain DSM 45956.
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R.S. performed experiments, data analysis, and manuscript drafting; N.B. carried out annotation, biosynthetic gene cluster analysis, supervised and corrected draft manuscript; A.M. assisted in the isolation of actinobacterial strains; M.D.H. corrected the manuscript and technical support; H-P.K. performed chemotaxonomic analysis, review and edited; I.N. supervised, analysed the data, and corrected the manuscript. All authors have read and agreed to the published version of the manuscript.
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Saker, R., Bouras, N., Meklat, A. et al. Genome-based reclassification of Actinopolyspora righensis Meklat et al. 2013 as a later heterotypic synonym of Actinopolyspora lacussalsi Guan et al. 2013 and description of Actinopolyspora lacussalsi subsp. lacussalsi subsp. nov. and Actinopolyspora lacussalsi subsp. righensis subsp. nov.. Arch Microbiol 204, 501 (2022). https://doi.org/10.1007/s00203-022-03120-4
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DOI: https://doi.org/10.1007/s00203-022-03120-4